Role of SHP-1, Kv.1.2, and cGMP in nitric oxide-induced ERK1/2 MAP kinase dephosphorylation in rat vascular smooth muscle cells

Cardiovasc Res. 2005 Nov 1;68(2):268-77. doi: 10.1016/j.cardiores.2005.05.031. Epub 2005 Jun 20.

Abstract

Objective: Nitric oxide (NO) elicits relaxation in vascular smooth muscle cells (VSMC) that is associated with guanylate cyclase (GC) and K(+) channel activation. In this study we determined the mechanisms that lead to ERK1/2 MAP kinase dephosphorylation in response to NO.

Methods: VSMC were treated with the NO donor SNAP or sodium nitroprusside (SNP), and ERK1/2, Src homology (SH) 1 domain-containing protein tyrosine phosphatase (SHP-1), and Kv.1.2 phosphorylation were assessed by immunoprecipitation and Western blot analysis.

Results: NO decreased basal ERK1/2 phosphorylation in a dose- and time-dependent manner. NO-induced ERK1/2 dephosphorylation was detected at 1 min and sustained for 30 min. Pre-treatment with the GC inhibitor ODQ or the protein tyrosine phosphatase inhibitor I prevented ERK1/2 dephosphorylation induced by SNAP. The inhibition of protein phosphatase 1A/2A had no effect on ERK1/2 dephosphorylation induced by SNAP. Treatment with cromakalim A, a nonspecific K(+) channel activator, also induced ERK1/2 dephosphorylation, while blockade of Kv.1.2 K(+) channels (AM92016 hydrochloride) prevented NO-induced ERK1/2 dephosphorylation. In addition, SNAP induced SHP-1 phosphorylation, and the Kv.1.2 dephosphorylation increase and SHP-1 phosphorylation was blocked by ODQ or AM92016. The basal interaction between ERK1/2 and SHP-1 was decreased in response to SNAP stimulation. SHP-1 also interacted with Kv.1.2 under basal conditions and participates in Kv.1.2 activation. Using the mouse mesenteric resistance artery, we found that ERK1/2 MAP kinase is involved in regulation of myogenic tone.

Conclusion: Thus, our study provides the first evidence that NO controls basal ERK1/2 phosphorylation by a signaling cascade that involves a dynamic signaling complex between cGMP, Kv.1.2 and SHP-1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Aorta, Thoracic
  • Blotting, Western / methods
  • Cells, Cultured
  • Cromakalim / pharmacology
  • Cyclic GMP / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Kv1.2 Potassium Channel / metabolism*
  • Male
  • Mitogen-Activated Protein Kinase Kinases / metabolism*
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism*
  • Nitric Oxide / pharmacology*
  • Nitric Oxide Donors / pharmacology
  • Nitroprusside / pharmacology
  • Okadaic Acid / pharmacology
  • Penicillamine / analogs & derivatives
  • Penicillamine / pharmacology
  • Phosphorylation / drug effects
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases / antagonists & inhibitors
  • Protein Tyrosine Phosphatases / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Vasodilator Agents / pharmacology

Substances

  • Enzyme Inhibitors
  • Intracellular Signaling Peptides and Proteins
  • Kv1.2 Potassium Channel
  • Nitric Oxide Donors
  • S-nitro-N-acetylpenicillamine
  • Vasodilator Agents
  • Cromakalim
  • Nitroprusside
  • Okadaic Acid
  • Nitric Oxide
  • Mitogen-Activated Protein Kinase Kinases
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Protein Tyrosine Phosphatases
  • Ptpn6 protein, mouse
  • Ptpn6 protein, rat
  • Penicillamine
  • Cyclic GMP